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Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation.

Publication ,  Journal Article
McConnell, GC; So, RQ; Grill, WM
Published in: Journal of neurophysiology
June 2016

Subthalamic nucleus (STN) deep brain stimulation (DBS) is an established treatment for the motor symptoms of Parkinson's disease (PD). However, the mechanisms of action of DBS are unknown. Random temporal patterns of DBS are less effective than regular DBS, but the neuronal basis for this dependence on temporal pattern of stimulation is unclear. Using a rat model of PD, we quantified the changes in behavior and single-unit activity in globus pallidus externa and substantia nigra pars reticulata during high-frequency STN DBS with different degrees of irregularity. Although all stimulus trains had the same average rate, 130-Hz regular DBS more effectively reversed motor symptoms, including circling and akinesia, than 130-Hz irregular DBS. A mixture of excitatory and inhibitory neuronal responses was present during all stimulation patterns, and mean firing rate did not change during DBS. Low-frequency (7-10 Hz) oscillations of single-unit firing times present in hemiparkinsonian rats were suppressed by regular DBS, and neuronal firing patterns were entrained to 130 Hz. Irregular patterns of DBS less effectively suppressed 7- to 10-Hz oscillations and did not regularize firing patterns. Random DBS resulted in a larger proportion of neuron pairs with increased coherence at 7-10 Hz compared with regular 130-Hz DBS, which suggested that long pauses (interpulse interval >50 ms) during random DBS facilitated abnormal low-frequency oscillations in the basal ganglia. These results suggest that the efficacy of high-frequency DBS stems from its ability to regularize patterns of neuronal firing and thereby suppress abnormal oscillatory neural activity within the basal ganglia.

Duke Scholars

Published In

Journal of neurophysiology

DOI

EISSN

1522-1598

ISSN

0022-3077

Publication Date

June 2016

Volume

115

Issue

6

Start / End Page

2791 / 2802

Related Subject Headings

  • Subthalamic Nucleus
  • Rats, Long-Evans
  • Pars Reticulata
  • Parkinsonian Disorders
  • Oxidopamine
  • Neurons
  • Neurology & Neurosurgery
  • Neural Inhibition
  • Microelectrodes
  • Methamphetamine
 

Citation

APA
Chicago
ICMJE
MLA
NLM
McConnell, G. C., So, R. Q., & Grill, W. M. (2016). Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation. Journal of Neurophysiology, 115(6), 2791–2802. https://doi.org/10.1152/jn.00822.2015
McConnell, George C., Rosa Q. So, and Warren M. Grill. “Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation.Journal of Neurophysiology 115, no. 6 (June 2016): 2791–2802. https://doi.org/10.1152/jn.00822.2015.
McConnell, George C., et al. “Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation.Journal of Neurophysiology, vol. 115, no. 6, June 2016, pp. 2791–802. Epmc, doi:10.1152/jn.00822.2015.

Published In

Journal of neurophysiology

DOI

EISSN

1522-1598

ISSN

0022-3077

Publication Date

June 2016

Volume

115

Issue

6

Start / End Page

2791 / 2802

Related Subject Headings

  • Subthalamic Nucleus
  • Rats, Long-Evans
  • Pars Reticulata
  • Parkinsonian Disorders
  • Oxidopamine
  • Neurons
  • Neurology & Neurosurgery
  • Neural Inhibition
  • Microelectrodes
  • Methamphetamine